Gallbladder wall thickening at ultrasonography: how to ...

Barbosa ABR et al. Gallbladder

REVIEW wall

ARTICLE

thickening

Gallbladder wall thickening at ultrasonography: how

to interpret it?*

Espessamento parietal da ves¨ªcula biliar no exame ultrassonogr¨¢fico: como interpretar?

Aldo Benjamim Rodrigues Barbosa1, Luis Ronan Marquez Ferreira de Souza2, Rog¨¦rio Silva

Pereira3, Giuseppe D¡¯Ippolito4

Abstract The present review was aimed at providing help for correct interpretation of gallbladder wall thickening and differential

diagnosis at ultrasonography. Gallbladder wall thickening is a frequent sonographic finding and has been subject of

great interest for being considered as a hallmark feature of acute cholecystitis, despite the fact that such a finding is

observed in a number of other medical conditions. An appropriate characterization and interpretation of this finding is

of great importance, considering that the correct diagnosis has a direct impact on the treatment that in some cases

includes surgery. In the present article, the authors describe a set of sonographic signs that, in association with clinical

and laboratory findings can reduce the number of diagnostic hypotheses allowing a more accurate establishment of

the cause for gallbladder wall thickening through a rational data evaluation.

Keywords: Gallbladder; Ultrasonography; Inflammation; Neoplasm.

Resumo O objetivo desta revis?o ¨¦ fornecer aux¨ªlio na interpreta??o correta do espessamento das paredes da ves¨ªcula biliar e

seus poss¨ªveis diagn¨®sticos diferenciais. O espessamento da ves¨ªcula biliar ¨¦ um achado frequente em exame de ultrassonografia e um tema de grande interesse, por ter sido considerado durante muito tempo como sinal espec¨ªfico de

colecistite aguda, apesar de se reconhecer que ocorre em uma s¨¦rie de outras situa??es cl¨ªnicas. A adequada caracteriza??o e interpreta??o desse achado ¨¦ de grande import?ncia, pois o diagn¨®stico correto tem impacto direto no

tratamento, que em alguns casos inclui interven??o cir¨²rgica. Neste artigo procuramos apresentar um conjunto de

sinais ultrassonogr¨¢ficos que, associados ao quadro cl¨ªnico e laboratorial do paciente, permitem restringir as alternativas diagn¨®sticas e estabelecer, com maior precis?o, a causa do espessamento parietal da ves¨ªcula biliar, atrav¨¦s de

uma avalia??o racional dos dados obtidos.

Unitermos: Ves¨ªcula biliar; Ultrassonografia; Inflama??o; Neoplasia.

Barbosa ABR, Souza LRMF, Pereira RS, D¡¯Ippolito G. Gallbladder wall thickening at ultrasonography: how to interpret it? Radiol Bras.

2011 Nov/Dez;44(6):381¨C387.

INTRODUCTION

Gallbladder wall thickening is a controversial topic among sonographers for being frequently found and for having been

considered, for a long time, a sign highly

suggestive acute cholecystitis. Such a con* Study developed at the Departments of Imaging Diagnosis

of Santa Casa de Miseric¨®rdia de Ituverava, Ituverava, SP, and

Universidade Federal do Tri?ngulo Mineiro (UFTM), Uberaba, MG,

Brazil.

1. MD, Radiologist at Santa Casa de Miseric¨®rdia de Ituverava,

Special Student, Course of Post-graduation in Pathology, Universidade Federal do Tri?ngulo Mineiro (UFTM), Uberaba, MG, Brazil.

2. PhD, Associate Professor, Universidade Federal do Tri?ngulo Mineiro (UFTM), Uberaba, MG, Brazil.

3. MD, Radiologist, Department of Imaging Diagnosis, Santa

Casa de Miseric¨®rdia de Ituverava, Ituverava, SP, Brazil.

4. Fellow PhD degree, Associate Professor, Department of

Imaging Diagnosis, Universidade Federal de S?o Paulo (Unifesp),

S?o Paulo, SP, Brazil.

Mailing Address: Dr. Luis Ronan M.F.de Souza. Radiologia e

Diagn¨®stico por Imagem. Avenida Frei Paulino, 30, Bairro Abadia.

Uberaba, MG, Brazil, 38080-793. E-mail: luisronan@

Received January 23, 2011. Accepted after revision June 3,

2011.

cept has been undergoing changes as a result of a greater experience of the professionals involved in imaging diagnosis and

the considerable technological development of ultrasonography (US) apparatuses(1).

Among the different diseases that cause

gallbladder walls thickening besides acute

cholecystitis, pancreatitis, diverticulitis,

heart failure, pyelonephritis and hepatitis

can be mentioned. The appropriate characterization and interpretation of such finding is of utmost importance, considering

that the correct diagnosis has a direct impact on the treatment and that in some cases

some of these diseases require surgical

approach(2).

Ultrasonography is the initial imaging

method for diagnostic approach and evaluation of the biliary system, as it is widely

available, safe, innocuous and non-expen-

Radiol Bras. 2011 Nov/Dez;44(6):381¨C387

0100-3984 ? Col¨¦gio Brasileiro de Radiologia e Diagn¨®stico por Imagem

sive. This method allows the detailed realtime study of the gallbladder, besides the

evaluation of other findings that contribute

to the final diagnosis, thus avoiding unnecessary cholecystectomies and their complications(3¨C5). Additionally, pre-operative US

(24 to 48 hours prior to surgery) may be

utilized as a safe and effective method to

avoid intraoperative endoscopic retrograde

cholangiopancreatography (IERC)(6). In the

present article, gallbladder wall thickening

is contextualized to guide its accurate interpretation in the light of clinical data and

to allow the choice of the appropriate therapeutic approach.

ANATOMY AND SONOGRAPHIC

TECHNIQUE

The gallbladder is a hollow pear-shaped

viscera with thin and regular walls, located

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Barbosa ABR et al. Gallbladder wall thickening

in the gallbladder fossa between the IV and

V segments of the liver, an area which is

devoid of the visceral peritoneum(7). The

gallbladder is divided into the infundibulum, body and fundus (Figure 1), and its

walls comprise four layers: a mucosa formed

by a simple columnar epithelium and by a

basal lamina; a second layer comprising

irregular muscular tissue; a third layer constituted by loose connective tissue; and a

last layer formed by the serosa(8¨C10). Its

function is to store the bile, and presents a

volume of 30 to 50 ml(6).

Gallbladder US is routinely performed

with a convex transducer. In order to acquire appropriate images, a systematic

scanning should be carried out with longitudinal and cross sectional views of the

organ, evaluating its shape, dimensions,

wall thickness, regularity and texture pattern of its walls and contents, besides

locoregional and Doppler velocimetric alterations(8). In order to assist the sonographic evaluation, the apparatuses are

equipped with resources that enhance the

methods accuracy, such as the harmonic

imaging, which allows increased lateral

resolution, signal-noise and contrast-noise

ratios(9).

Sonographic images provide a faithful

representation of the gallbladder which can

be correlated with its anatomical structure.

By means of US it is possible to identify

three layers: the innermost, corresponding

to the mucosa, that is linear, echogenic and

presents a regular surface; the second one,

corresponding to the muscular layer, is thin

and slightly hypoechoic; and outermost

layer corresponding to the organ¡¯s serosa,

that is linear, echogenic and regular(1,9).

According to several authors(1,2), the upper limit for normality of the gallbladder

wall thickness is 3 mm. However, in patients under inappropriate fasting, the parietal thickness may exceed such a limit

because of the organ¡¯s smooth muscle contraction(8). So, 8-hour fasting before the examination is recommended, particularly in

cases where the gallbladder is the focus of

the study. The main differential diagnosis

of parietal thickening is that of functional

changes of the organ, in which one observes a persistently withered gallbladder,

even at a re-evaluation after extended fasting(9). Another cause of ¡°pseudothick-

382

Figure 1. Laparoscopic anatomy (a,b,c) compared with sonographic anatomy (d) demonstrating gallbladder infundibulum, body and fundus.

ening¡± is related to erroneous insonation by

the transducer. In this case, the performance

of maneuvers changing the decubitus is

useful in the correct definition of the gallbladder wall thickness. An important differential diagnosis in these cases is the

functional change of the gallbladder (10,11)

(Figure 2).

Gallbladder wall thickening is classified as mild (between 4 and 7 mm), marked

(> 7 mm), and in focal or diffuse. As a rule,

systemic diseases such as heart, renal or

hepatic failure cause diffuse and less marked

thickening, contrary to tumor lesions that

cause focal and more exuberant thickening,

a

frequently greater than 10 mm(7). The presence of some associated signs allows the

observer to direct the diagnosis towards a

more specific etiology(9¨C11). Among such

signs, the following can be mentioned: biliary tract dilation, presence of a static gallstone, perivesicular fluid, hilar lymph node

enlargement, perivesicular fat heterogeneity and increased gallbladder transverse

diameter. The disorders that cause gallbladder wall thickening may be classified as inflammatory, neoplastic and systemic, and

their differentiation may be obtained by

means of a combined evaluation of clinical and imaging findings.

b

Figure 2. Patient with dyspepsia. Observe the withered gallbladder with thickened wall (arrow) at the first

evaluation (a), appearance which is maintained after 12-hour fasting (arrowheads on b). The sonographic

appearance suggests gallbladder dysmotility.

Radiol Bras. 2011 Nov/Dez;44(6):381¨C387

Barbosa ABR et al. Gallbladder wall thickening

Acute calculous cholecystitis

It is the most common inflammatory

complication that affects the gallbladder,

and is related to choledocholithiasis in 90¨C

95% of the cases. It is the fourth most common cause of acute abdomen requiring hospitalization(3). In 95% of cases it is caused

by persistent obstruction by stones in the

infundibulum or in the cystic duct. In spite

of not being pathognomonic, acute calculous cholecystitis is the main cause of gallbladder wall thickening at US. In general,

the gallbladder wall is less than 7 mm thick,

presenting regular contour and trilaminar

appearance(3,9,11). Such echotextural appearance of the gallbladder walls may

change, for example in cases of emphysematous cholecystitis, where echogenic parietal images with acoustic reverberation

compatible with gas are observed(12) (Figure 3).

Other sonographic findings are important, as they increase the method specificity, such as: impacted calculus in the common bile duct with upstream dilatation, infundibular calculi, tense gallbladder with

a transverse diameter > 4 cm (hydrops of

the gallbladder), positive painful decompression at the cystic point (sonographic

Murphy¡¯s sign), presence of perivesicular

fluid and hyperflow from its walls at Doppler(5) (Figure 4).

The US sensitivity ranges between 80%

and 100%, and specificity ranges between

60% and 100%. The positive predictive

value in the identification of calculi is 88%,

increasing to 92% as associated with

sonographic Murphy¡¯s sign. Gallbladder

wall thickening associated with the

Murphy¡¯s sign has a predictive value of up

to 94%(11,12).

Another rare condition that determines

gallbladder wall thickening associated with

inflammatory process is the Mirizzi syndrome. In such a situation, an impacted

gallstone located in the gallbladder neck or

in the cystic duct causes dilatation of the

biliary tract, causing compression of the

common hepatic duct or secondary inflammation, producing edema or fibrosis on the

duct wall. At US, besides the impacted

calculus, one observes a distal common

bile duct with normal caliper, peribiliary

Radiol Bras. 2011 Nov/Dez;44(6):381¨C387

inflammatory signs and gallbladder wall

thickening, similar to acute cholecystitis.

Magnetic resonance imaging (MRI) and

MRI cholangiography are very useful in

such cases, particularly to rule out the pres-




INFLAMMATORY CAUSES

Figure 3. Emphysematous cholecystitis. Observe

echogenic parietal images of the gallbladder, with

reverberation compatible with gas (arrow).

a

ence of a pancreatic head tumor or primary

sclerosing cholangitis(11) (Figure 5).

Chronic calculous cholecystitis

It consists of an inflammatory process

of the gallbladder, originated from a transitory gallbladder obstruction, causing inflammation and fibrosis(11,12). Porcelain

gallbladder is a rare presentation of chronic

cholecystitis, where the gallbladder walls

are partially or completely calcified. In

spite of the lack of consensus, many authors consider that the inflammatory process represents a risk factor for gallbladder

carcinoma, and, even being it an accidental finding in asymptomatic patients submitted to routine US examinations, many

advocate the prophylactic cholecystectomy(1,3,13) (Figure 4).

b

Figure 4. Female, 45-year-old patient with severe abdominal pain in the right hypochondrium, irradiating to the scapular region. Positive sonographic Murphy¡¯s sign. Figures (a,b) demonstrate tense gallbladder with thickened walls and presence of gallstones.

a

b

Figure 5. Mirizzi syndrome. a: Oblique coronal T2-weighted sequence. b: MRI cholangiography with volume rendering. In this case, the presence of impacted gallstone in the cystic duct, causing dilatation of

the biliary tract and compression of the common hepatic duct.

383

Barbosa ABR et al. Gallbladder wall thickening

Acalculous cholecystitis

Acalculous cholecystitis is an uncommon and severe entity, affecting patients

with diabetes and in poor general conditions. It is more common in hospitalized

patients (undergoing mechanical ventilation and hyperalimentation therapy) and

trauma victims, or in extensive burn patients, with a high mortality rate. Such a

condition was described in 1970, in seriously wounded soldiers during the Vietnam

war(14).

During the interpretation of the sonographic findings, i.e., gallbladder wall thickening, tense and distended gallbladder, and

presence of perivesicular fluid, the correlation with the clinical context is of utmost

importance for a correct diagnosis(3,14). The

absence of sonographic Murphy¡¯s sign does

not rule out the diagnosis(14,15) (Figure 6).

Figure 6. Acalculous cholecystitis. Observe diffuse

gallbladder wall thickening, with flow at color Doppler and a minor, adjacent fluid collection. All these

findings are frequently observed in cholecystitis, and

in the present case is not associated with the presence of gallstones.

Acalculous cholecystitis is frequently

misdiagnosed, as some sonographers

equivocally attribute to chronic acalculous

cholecystitis, the secondary thickening determined by systemic pathologies such as

pyelonephritis(16), for example. Another

common erroneous interpretation occurs in

cases of acute cholecystitis caused by nonvisualized small obstructive calculi in the

common bile duct(3) (Figure 7).

Xanthogranulomatous cholecystitis

It is an uncommon pathology, described

in the early 1980¡¯s as a pseudotumor presentation of chronic calculous cholecystitis, secondary to bile extravasation through

the gallbladder walls, frequently associated

384

a

b

Figure 7. Diffuse and unilateral pyelonephritis. Upper abdominal US (a) did not identify gallstones or

increase in gallbladder¡¯s diameter, however the walls were thickened. At contrast-enhanced abdominal

CT (b), heterogeneous nephrogram and increased volume of the right kidney are observed, leading to

gallbladder wall thickening (arrow).

with adenocarcinoma(17,18). At macroscopic

examination, one observes a nodular thickening of the walls in association with the

presence of calculi and possible locoregional infiltration. Lymph nodes enlargement and coexistence with gallbladder cancer may also be found.

Its main sonographic sign is diffuse

gallbladder wall thickening, besides hypoechoic nodules, which may be found in up

to 35% of the patients(3,17,18). Such cases

may be undistinguishable from the infiltrative presentation of gallbladder carcinoma(18). Clinically, it manifests with a

clinical picture of cholecystitis in women

aged from 60 to 70 years.

Adenomyomatosis of the gallbladder

It is characterized by excessive proliferation of the surface epithelium towards

the Rokitansky-Aschoff sinuses, determining wall thickening that may be focal, segmental or diffuse(5). The main sonographic

presentation corresponds to segmental parietal thickening with multiple echogenic

intramural foci, which cause posterior reverberation artifacts, known as comet-tail

artifacts. Other signs such as gallbladder

distension, presence of perivesicular fluid

or positive sonographic Murphy¡¯s sign are

not observed(3,18).

It is a benign non-inflammatory condition of the gallbladder, found in 8.7% of the

cholecystectomies(5). It manifests with persistent pain in the right hypochondrium,

and is most commonly found in women, in

association with gallstones in 90% of the

cases. Upon symptoms persistence, cholecystectomy is indicated(5,15).

Cholesterol polyp

Focal and nodular gallbladder wall

thickening represent approximately 50% of

all polypoid lesions, and most of the times

do not present a malignant potential(1). The

patients do not present any symptoms and

at US, a static echogenic well defined

nodular image is identified. The main differential diagnoses include adenoma and

adenocarcinoma(1,19).

Two-dimensional US is not capable of

differentiating small neoplastic polypoid

lesions from non-neoplastic ones, but some

studies have demonstrated the usefulness

of three-dimensional US in the differential

diagnosis between polyps (Figure 8). In

such cases, MRI may be very useful in that

differentiation(20).

Porcelain gallbladder

It is an uncommon chronic cholecystitis variation characterized by extensive cal-

Figure 8. Gallbladder cholesterolosis with polypoid

image in the fundus. Echogenic points with reverberation on the gallbladder walls, corresponding to

cholesterolosis (arrowheads) associated with polypoid lesion in the gallbladder fundus (arrow).

Radiol Bras. 2011 Nov/Dez;44(6):381¨C387

Barbosa ABR et al. Gallbladder wall thickening

cification of the gallbladder walls, which

can be partially or completely affected. The

term ¡°porcelain¡± is utilized because of its

consistency and appearance (Figure 9). Its

prevalence in cholecystectomies is 0.06%

to 0.8%. In 95% of cases, association with

cholelithiasis is found. It is five times more

common in women than in men, and is most

frequent in the fifth and sixth decades of

life(7,12). Early in the 20th century, one believed that there was an association with

neoplasia, but most recently, studies have

not confirmed the initial findings, thus demonstrating a low incidence of coexistence

of neoplasia with porcelain gallbladder(20,21).

NEOPLASTIC CAUSES

Gallbladder carcinoma

It is the most common neoplasia of the

biliary system, with 2.5 new cases per

100,000 inhabitants per year. It has a high

mortality rate as its diagnosis is most of

a

times achieved at advanced stages of the

disease, because of the scarcity of symptoms. When present, the initial symptoms

are nonspecific and include weight loss,

abdominal pain, fever and jaundice(1,2,7,16)

and are frequently associated with the presence of calculi (73% to 98%)(6). Only 1%

of the cholecystectomies performed for

cholelithiasis result in incidental finding of

gallbladder carcinoma(2). The most significant risk factor is the presence of chronic

inflammatory process usually triggered by

the calculi. The main differential diagnoses

include complicated acute cholecystitis,

hepatocellular carcinoma and metastasis to

the gallbladder fossa.

Adenocarcinoma is the malignant histological type of tumor that most frequently

affects the gallbladder, occurring in 90% of

cases. Such tumor generally presents three

image patterns: a) mass occupying and

obscuring the gallbladder bed; b) focal or

diffuse parietal thickening; c) polypoid

parietal lesion projecting towards its lumen. Its most frequent presentation is a

large solid lesion in the gallbladder fossa

in association with calculi and extending to

the liver and adjacent organs (Figure 10).

When focal or asymmetric wall thickening > 10 mm is found, the possibility of

neoplasia is high. In such cases the characterization of other factors such as locoregional lymph nodes enlargement enhances the diagnostic hypothesis. Computed tomography (CT) presents a characteristic enhancement pattern that is typical

of lesions suspicious for malignancy, with

iodinated contrast uptake in the arterial

phase, becoming isodense in the equilibrium phase(22,23). Magnetic resonance imaging demonstrates hyperintense and heterogeneous images on T2-weighted sequences and hypointense on T1-weighted

sequences, with post-contrast enhancement. In the cases of diffuse thickening

with uniform infiltration, its imaging appearance is similar to that of chronic cholecystitis(21).

The accurate differentiation between

malignant and benign polypoid lesions cannot be made by means of US alone. Generally, malignant polyps are > 1 cm and

seldom present calcification and necrosis.

They present early and prolonged contrast

uptake after administration of gadolinium,

contrary to benign lesions, which present

early contrast uptake with subsequent

washout(21¨C23).

b

Metastasis to the gallbladder

Figure 9. Abdominal US and radiograph of a 50-year-old patient presenting with abdominal discomfort.

Observe porcelain gallbladder (arrows), with thin calcifications on its wall.

a

b

Some tumors, such as carcinoid tumor,

lymphoma, breast carcinoma and sarcomas

c

Figure 10. Gallbladder carcinoma associated with lithiasis. Observe dilatation of intrahepatic biliary ducts (a ¨C arrows), lymph node enlargement in the hepatic

hilum (b ¨C arrow) and ill-defined lesion associated with gallstones (c).

Radiol Bras. 2011 Nov/Dez;44(6):381¨C387

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